Skip to main content

Differences in functional activity between boys with pure oppositional defiant disorder and controls during a response inhibition task: a preliminary study

Abstract

Functional Magnetic Resonance Imaging (fMRI) of inhibitory control has only been investigated in patients with attention deficit hyperactivity disorder (ADHD) and conduct disorder (CD). The objective of this study was to investigate the differences of functional areas associated with inhibitory control between boys with pure oppositional defiant disorder (ODD) and controls during a response inhibition task using functional magnetic resonance imaging (fMRI). Eleven boys with pure ODD and ten control boys, aged 10 to 12, performed a GoStop response inhibition task in this study. The task has a series of “go” trials to establish a pre-potent response tendency and a number of “stop” trials to test subjects’ ability to withhold their responses. During the GoStop task, greater activation in the dorsolateral parts of the bilateral inferior frontal gyrus, left middle frontal gyrus (lMFG) and right superior frontal gyrus (rSFG) activation was seen in the ODD boys. Additionally, reduced activation in regions of the right inferior frontal gyrus (rIFG) was seen in the ODD boys in comparison with the control group. The results may suggest that the higher activation in areas adjacent to the rIFG could be the cause of reduced activation in the rIFG; although this is speculative and requires additional supporting evidence. The findings further suggest that ODD is a less pronounced functional disorder compared to ADHD and CD.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Aron, A. R., & Poldrack, R. A. (2005). The cognitive neuroscience of response inhibition: relevance for genetic research in attention-deficit/hyperactivity disorder. Biological Psychiatry, 57(11), 1285–1292.

    PubMed  Article  Google Scholar 

  • Aron, A. R., & Poldrack, R. A. (2006). Cortical and subcortical contributions to stop signal response inhibition: role of the subthalamic nucleus. Journal of Neuroscience, 26(9), 2424–2433.

    CAS  PubMed  Article  Google Scholar 

  • Aron, A. R., Fletcher, P. C., Bullmore, E. T., Sahakian, B. J., & Robbins, T. W. (2003). Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans. Nature Neuroscience, 6(2), 115–116.

    CAS  PubMed  Article  Google Scholar 

  • Aron, A. R., Robbins, T. W., & Poldrack, R. A. (2004). Inhibition and the right inferior frontal cortex. Trends in Cognitive Sciences, 8(4), 170–177.

    PubMed  Article  Google Scholar 

  • Barkley, R. A. (1997). ADHD and the nature of self-control. New York: Guilford.

    Google Scholar 

  • Barratt, E. S., & Slaughter, L. (1998). Defining, measuring, and predicting impulsive aggression: a heuristic model. Behavioral Sciences and the Law, 16, 285–302.

    CAS  PubMed  Article  Google Scholar 

  • Behrens, T. E., Johansen-Berg, H., Woolrich, M. W., Smith, S. M., Wheeler-Kingshott, C. A., Boulby, P. A., et al. (2003). Noninvasive mapping of connections between human thalamus and cortex using diffusion imaging. Nature Neuroscience, 6, 750–757.

    CAS  PubMed  Article  Google Scholar 

  • Biederman, J., Faraone, S. V., Milberger, S., Jetton, J. G., Chen, L., Mick, E., et al. (1996). Is childhood oppositional defiant disorder a precursor to adolescent conduct disorder? Finding from a four-year follw-up study of children with ADHD. Journal of American Academy of Child and Adolescent Psychiatry, 35(9), 1193–1204.

    CAS  Article  Google Scholar 

  • Bjork, J. M., Dougherty, D. M., Moeller, F. G., Harper, R. A., Scott-Gurnell, K., & Swann, A. C. (2002). Laboratory measures of impulsivity in hospitalized adolescents with disruptive behavior disorders. Biological Psychiatry, 47, 489.

    Google Scholar 

  • Booth, J. R., Burman, D. D., Meyer, J. R., Lei, Z., Trommer, B. L., Davenport, N. D., et al. (2005). Larger deficits in brain networks for response inhibition than for visual selective attention in attention deficit hyperactivity disorder (ADHD). Journal of Child Psychology and Psychiatry, 46, 94–111.

    PubMed  Article  Google Scholar 

  • Castellanos, F. X., Sonuga-Barke, E. J. S., Milham, M. P., & Tannock, R. (2006). Characterizing cognition in ADHD: beyond executive dysfunction. Trends in Cognitive Science, 10, 117–123.

    Article  Google Scholar 

  • Chao, H., Luo, X., Chang, J.L.K., Li, R. (2009). Activation of the pre-supplementary motor area but not inferior prefrontal cortex in association with short stop signal reaction time – an intra-subject analysis. BMC Neuroscience, 10(75). doi:10.1186/1471-2202-10-75

  • Dodge, K. A. (1993). Social-cognitive mechanisms in the development of conduct disorder and depression. Annual Review of Psychology, 44, 559–584.

    CAS  PubMed  Article  Google Scholar 

  • Dougherty, D. M., Bjork, J. M., Harper, R. A., Marsh, D. M., Moeller, F. G., Mathias, C. W., et al. (2003). Behavioral impulsivity paradigms: a comparison in hospitalized adolescents with disruptive behavior disorders. Journal of Child Psychology and Psychiatry, 44(8), 1145–1157.

    Google Scholar 

  • Duann, J. R., Ide, J. S., Luo, X., & Li, R. (2009). Functional connectivity delineates distinct roles of the inferior frontal cortex and presupplementary motor area in stop signal inhibition. Journal of Neuorscience, 29(32), 10171–10179.

    CAS  Article  Google Scholar 

  • Durston, S., Mulder, M., Casey, B. J., Ziermans, T., & van Engeland, H. (2006). Activation in ventral prefrontal cortex is sensitive to genetic vulnerability for attention-deficit hyperactivity disorder. Biological Psychiatry, 60, 1062–1070.

    CAS  PubMed  Article  Google Scholar 

  • Evenden, J. L. (1999). Varieties of impulsivity. Psychopharmacology (Berlin), 146(4), 348–361.

    CAS  Article  Google Scholar 

  • Friston, K. J., Holmes, A. P., & Worsley, K. J. (1995). Statistical parametric maps in functional imaging: a general linear model approach. Human Brain Mapping, 2, 189–210.

    Article  Google Scholar 

  • Garavan, H., Ross, T. J., & Stein, E. A. (1999). Right hemispheric dominance of inhibitory control: an event-related fMRI study. Proceedings of National Academy of Sciences, 96, 8301–8306.

    CAS  Article  Google Scholar 

  • Hampshire, A., Chamberlain, S. R., Monti, M. M., Duncan, J., & Owen, A. M. (2010). The role of the right inferior frontal gyrus: inhibition and attentional control. NeuroImage, 50, 1313–1319.

    PubMed Central  PubMed  Article  Google Scholar 

  • Hendren, R. L., Backer, I. D., & Pandina, G. J. (2000). Review of neuroimaging studies of child and adolescent psychiatric disorders from the past 10 years. Journal of American Academy of Child and Adolescent Psychiatry, 39(7), 815–828.

    CAS  Article  Google Scholar 

  • Hill, J. (2002). Biological, psychological and social processes in the conduct disorders. Journal of Child Psychology and Psychiatry, 43, 133–164.

    PubMed  Article  Google Scholar 

  • Hummer, T. A., Kronenberger, W. G., Wang, Y., Dunn, D. W., Mosier, K. M., Kalnin, A. J., et al. (2011). Executive functioning characteristics associated with ADHD comorbidity in adolescents with disruptive behavior disorder. Journal of Abnormal Child Psychology, 39, 11–19.

    PubMed  Article  Google Scholar 

  • Konishi, S., Nakajima, K., Uchida, I., Kikyo, H., Kameyama, M., & Miyashita, Y. (2002). Common inhibitory mechanism in human inferior prefrontal cortex revealed by event-related functional MRI. Brain, 122, 981–991.

    Article  Google Scholar 

  • Konrad, K., Neufang, S., Hanisch, C., Fink, G. R., & Herpertz-Dahlmann, B. (2006). Dysfunctional attentional networks in children with attention deficit/hyperactivity disorder: evidence from an event-related functional magnetic resonance imaging study. Biological Psychiatry, 59(7), 643–651.

    PubMed  Article  Google Scholar 

  • Kuperman, S., Schlosser, S. S., Kramer, J. R., Bucholz, K., Hesselbrock, V., Reich, T., et al. (2001). Developmental sequence from disruptive behavior diagnosis to adolescent alcohol dependence. American Journal of Psychiatry, 158(12), 2022–2026.

    CAS  PubMed  Article  Google Scholar 

  • Lavigne, J. V., Cicchetti, C., Gibbons, R. D., Binns, H. J., Larsen, L., & DeVito, C. (2001). Oppositional defiant disorder with onset in preschool years: longitudinal stability and pathways to other disorders. Journal of American Academy of Child and Adolescent Psychiatry, 40(12), 1393–1400.

    CAS  Article  Google Scholar 

  • Li, R., Huang, C., Constable, T., & Sinha, R. (2006). Imaging response inhibition in a stop-signal task: neural correlates independent of signal monitoring and post-response processing. Journal of Neuroscience, 26(1), 186–192.

    CAS  PubMed  Article  Google Scholar 

  • Loeber, R., & Birmaher, B. (2002). Oppositional defiant disorder and conduct disorder: a review of the past 10 years, part II. Journal of American Academy of Child and Adolescent Psychiatry, 41(11), 1275–1293.

    Article  Google Scholar 

  • Loeber, R., Burke, J. D., Lahey, B. B., Winters, A., & Zera, M. (2000). Oppositional defiant and conduct disorder: a review of the past 10 years, part I. Journal of American Academy of Child and Adolescent Psychiatry, 39(12), 1468–1484.

    CAS  Article  Google Scholar 

  • Marsh, D. M., Dougherty, D. M., Mathias, C. W., Moeller, F. G., & Hicks, L. R. (2002). Comparison of women with high and low trait impulsivity using laboratory impulsivity models of response-disinhibition and reward-choice. Personality and Individual Differences, 33, 1291–1310.

    Article  Google Scholar 

  • Martinussen, R., Hayden, J., Hogg-Johnson, S., & Tannock, R. (2005). A meta-analysis of working memory impairments in children with attention deficit/hyperactivity disorder. Journal of American Academy of Child and Adolescent Psychiatry, 44, 377–384.

    Article  Google Scholar 

  • Menon, V., Adleman, N. E., White, C. D., Glover, G. H., & Reiss, A. L. (2001). Errorrelated brain activation during a Go/NoGo response inhibition task. Human Brain Mapping, 12, 131–143.

    CAS  PubMed  Article  Google Scholar 

  • Nigg, J. T. (2000). On inhibition/disinhibition in developmental psychopathology: views from cognitive and personality psychology and working inhibition taxonomy. Psychological Bulletin, 126, 220–246.

    CAS  PubMed  Article  Google Scholar 

  • Oosterlaan, J., Logan, G. D., & Sergeant, J. A. (1998). Response inhibition in AD/HD, CD, comorbid AD/HD+CD, anxious, and control children: a meta-analysis of studies with the stop task. Journal of Child Psychology and Psychiatry, 39, 411–425.

    CAS  PubMed  Article  Google Scholar 

  • Oosterlaan, J., Scheres, A., & Sergeant, J. A. (2005). Which executive functioning deficits are associated with AD/HD, ODD/CD and comorbid AD/HD+ODD/CD? Journal of Abnormal Child Psychology, 33, 69–85.

    PubMed  Article  Google Scholar 

  • Pliszka, S. R., Lancaster, J., Liotti, M., & Semrud-Clikeman, M. (2006). Volumetric MRI differences in treatment-naïve vs. chronically treated children with ADHD. Neurology, 67(6), 1023–1027.

    PubMed  Article  Google Scholar 

  • Rubia, K., Smith, A. B., Brammer, M. J., & Taylor, E. (2003). Right inferior prefrontal cortex mediates response inhibition while mesial prefrontal cortex is responsible for error detection. NeuroImage, 20, 351–358.

    PubMed  Article  Google Scholar 

  • Rubia, K., Smith, A. B., Brammer, M. J., Toone, B., & Taylor, E. (2005). Abnormal brain activation during inhibition and error detection in medication-naive adolescents with ADHD. American Journal of Psychiatry, 162(6), 1067–1075.

    PubMed  Article  Google Scholar 

  • Rubia, K., Smith, A. B., Brammer, M., & Taylor, E. (2007a). Performance of children with attention deficit hyperactivity disorder (ADHD) on a test battery for impulsiveness. Child Neuropsychology, 13, 276–304.

    PubMed  Article  Google Scholar 

  • Rubia, K., Smith, A. B., Taylor, E., & Brammer, M. (2007b). Linear age-correlated functional development of right inferior fronto-striato cerebellar networks during response inhibition and anterior cingulate during error-related processes. Human Brain Mapping, 28(11), 1163–1177.

    PubMed  Article  Google Scholar 

  • Rubia, K., Halari, R., Smith, A., Mohammed, M., Scott, S., Giampoetro, V., et al. (2008). Dissociated functional Brain abnormalities of inhibition in boys with pure conduct disorder and in boys with pure attention deficit hyperactivity disorder. American Journal of Psychiatry, 165, 889–897.

    PubMed  Article  Google Scholar 

  • Rubia, K., Halari, R., Smith, A., Mohammad, M., Scott, S., & Brammer, M. (2009a). Shared and disorder-specific prefrontal abnormalities in boys with pure attention-deficit/hyperactivity disorder compared to boys with pure CD during interference inhibition and attention allocation. Journal of Child Psychology and Psychiatry, 50, 669–678.

    PubMed  Article  Google Scholar 

  • Rubia, K., Smith, A., Halari, R., Matukura, F., Mohammad, M., Taylor, E., et al. (2009b). Disorder-specific dissociationof orbito- frontal dysfunction in boys with pure conduct disorder during reward and ventrolateral prefrontal dysfunction in boys with pure attention-deficit/hyperactivity disorder during sustained attention. American Journal of Psychiatry, 166, 83–94.

    PubMed  Article  Google Scholar 

  • Rubia, K., Smith, A., Halari, R., Cubillo, A., Mohammad, M., Brammer, M., et al. (2009c). Methylphenidate normalizes activation and functional connectivity deficits in attention and motivation networks in medication-naïve children with ADHD during a rewarded continuous performance task. Neuropharmacology, 57(7), 640–652.

    CAS  PubMed  Article  Google Scholar 

  • Schachar, R., & Tannock, R. (1995). Test of four hypotheses for the comorbidity of attention-deficit hyperactivity disorder and conduct disorder. Journal of the American Academy of Child and Adolescent Psychiatry, 34, 639–648.

    CAS  PubMed  Article  Google Scholar 

  • Sergeant, J. A., Geurts, H., & Oosterlaan, J. (2002). How specific is a deficit of executive functioning for attention-deficit/hyperactivity disorder? Behavioural Brain Research, 130, 3–28.

    PubMed  Article  Google Scholar 

  • Silk, T., Vance, A., Rinehart, N., & Egan, G. (2005). Fronto-parietal activation in attention-deficit hyperactivity disorder, combined type: functional magnetic resonance imaging study The. British Journal of Psychiatry, 187, 282–283.

    CAS  PubMed  Article  Google Scholar 

  • Snyder, J., Schrepferman, L., & St Peter, C. (1997). Origins of antisocial behavior. Negative reinforcement and affect dysregulation of behavior as socialization mechanisms in family interaction. Behavior Modification, 21(2), 187–215.

    CAS  PubMed  Article  Google Scholar 

  • Speltz, M. L., McClellan, J., DeKlyen, M., & Jones, K. (1999). Preschool boys with oppositional defiant disorder: clinical presentation and diagnostic change. Journal of American Academy of Child and Adolescent Psychiatry, 38(7), 838–845.

    CAS  Article  Google Scholar 

  • Swann, A. C., Bjork, J. M., Moeller, F. G., & Dougherty, D. M. (2002). Two models of impulsivity: relationship to personality traits and psychopathology. Biological Psychiatry, 51(12), 988–994.

    PubMed  Article  Google Scholar 

  • Van Goozen, S. H., Van den Ban, E., Matthys, W., Cohen-Kettenis, P. T., Thijssen, J. H., & Van Engeland, H. (2000). Increased adrenal androgen functioning in children with oppositional defiant disorder: a comparison with psychiatric and normal controls. Journal of American Academy of Child and Adolescent Psychiatry, 39(11), 1446–1451.

    Article  Google Scholar 

  • Zhu, Y., Su, L. Y., & Liu, P. Z. (2005). A study of behavioral problems in oppositional defiant disorder. Chinese Journal of Psychiatry, 38(4), 218–221.

    Google Scholar 

  • Zhu, Y., Su, L. Y., Wei, Z., & Zhou, M. (2008). Study on impulsivity features of oppositional defiant disorder in children. Chinese Journal of Child Health Care, 16(6), 641–643.

    Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Kui Ying.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Zhu, Y., Ying, K., Wang, J. et al. Differences in functional activity between boys with pure oppositional defiant disorder and controls during a response inhibition task: a preliminary study. Brain Imaging and Behavior 8, 588–597 (2014). https://doi.org/10.1007/s11682-013-9275-7

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11682-013-9275-7

Keywords

  • Oppositional defiant disorder (ODD)
  • Right inferior frontal gyrus (rIFG)
  • Functional magnetic resonance imaging (fMRI) response inhibition task